Photo. Point-intercept abundance measurements of vascular plant species in the Guisveld lowland SphagnumPhragmites reedland.
Plant Ecology (2006) 182:13 –24
DOI 10.1007/s11258-005-9028-9
Springer 2006
Vascular plant responses to elevated CO2 in a temperate lowland Sphagnum
peatland
Rubén Milla1,2, Johannes H.C. Cornelissen1,*, Richard S.P. van Logtestijn1, Sylvia
Toet1,3 and Rien Aerts1
1
Department of Systems Ecology, Institute of Ecological Sciences Faculty of Earth and Life Sciences, Vrije
Universiteit, De Boelelaan 1085, Amsterdam, 1081, HV, The Netherlands; 2Instituto Pirenaico de Ecologı´a
(CSIC), P.O. Box 202, 50080, Zaragoza, Spain; 3Environment Department, University of York Heslington,
York, YO10 5DD, United Kingdom; *Author for correspondence: (e-mail: hans.cornelissen@
ecology.falw.vu.nl; fax: +31-(0)20-4447123)
Received 1 September 2004; accepted in revised form 15 December 2004
Key words: CO2-enrichment, FACE, Litter respiration, Nutrient resorption, Species abundance,
Sphagnum, The Netherlands
Abstract
Vascular plant responses to experimental enrichment with atmospheric carbon dioxide (CO2), using
MINIFACE technology, were studied in a Dutch lowland peatland dominated by Sphagnum and
Phragmites for 3 years. We hypothesized that vascular plant carbon would accumulate in this peatland in
response to CO2 enrichment owing to increased productivity of the predominant species and poorer quality
(higher C/N ratios) and consequently lower decomposability of the leaf litter of these species. Carbon
isotope signatures demonstrated that the extra 180 ppmv CO2 in enriched plots had been incorporated into
vegetation biomass accordingly. However, on the CO2 sequestration side of the ecosystem carbon budget,
there were neither any significant responses of total aboveground abundance of vascular plants, nor of any
of the individual species. On the CO2 release side of the carbon budget (decomposition pathway), litter
quantity did not differ between ambient and CO2 treatments, while the changes in litter quality (N and P
concentration, C/N and C/P ratio) were marginal and inconsistent. It appeared therefore that the afterlife
effects of significant CO2-induced changes in green-leaf chemistry (lower N and P concentrations, higher
C/N and C/P) were partly offset by greater resorption of mobile carbohydrates from green leaves during
senescence in CO2-enriched plants. The decomposability of leaf litters of three predominant species from
ambient and CO2-enriched plots, as measured in a laboratory litter respiration assay, showed no differences. The relatively short time period, environmental spatial heterogeneity and small plot sizes might
explain part of the lack of CO2 response. When our results are combined with those from other Sphagnum
peatland studies, the common pattern emerges that the vascular vegetation in these ecosystems is genuinely
resistant to CO2-induced change. On decadal time-scales, water management and its effects on peatland
hydrology, N deposition from anthropogenic sources and land management regimes that arrest the early
successional phase (mowing, tree and shrub removal), may have a greater impact on the vascular plant
species composition, carbon balance and functioning of lowland Sphagnum –Phragmites reedlands than
increasing CO2 concentrations in the atmosphere.
14
Introduction
Global atmospheric CO2 concentrations have
steadily risen from 280 ppm before the Industrial
Revolution to 370 ppm currently and 560 ppm
will be reached by the end of the 21st century
according to most predictions (IPCC 2001). Peatlands store a substantial proportion of the global
organic carbon pool (Gorham 1991), which is a
consequence of a long-term greater productivity
compared to decomposition rates. Higher atmospheric CO2 concentrations could potentially
change the balance between productivity and
decomposition of peatlands, which could have
major repercussions for large-scale carbon budgets. In this paper, we investigate how elevated
CO2 affects the vascular plant contributions to this
balance (see Toet et al. In press, for moss contributions to this balance). So far responses in terms
of productivity or plant growth have been found
to be very limited in realistic in situ experiments
with CO2 enrichment in temperate northern ombrotrophic peatlands, both for the dominant
peatland moss Sphagnum and vascular plants
(Berendse et al. 2001; Hoosbeek et al. 2001;
Heijmans et al. 2002). However, to our knowledge
there is no information on productivity related
responses of vascular plants in partly minerotrophic temperate lowland Sphagnum –Phragmites
reedlands. In such peatlands, a relatively thin
mostly rain-fed and nutrient-poor Sphagnum layer
sits on top of a muddy, more nutrient-rich layer
fed mostly by the groundwater, which is in contact
with surrounding canals and ditches. While
lowland peatlands in general are widespread
throughout the temperate northern hemisphere,
Sphagnum –Phragmites reedlands, which were once
more widespread in the western Netherlands and
other coastal parts of NW Europe, are now restricted to some nature reserves, mainly in The
Netherlands. These peatlands have great conservation value as rare ecosystems with unique compositions of species, several of which are
themselves rare or under threat internationally. In
these ecosystems, the roots of the predominant
vascular plants, including Phragmites australis
reed, penetrate into this deeper, richer soil horizon.
In ombrotrophic peatlands, the lack of CO2
growth responses may be explained partly by the
strong constraint imposed by low nutrient availability, as has been reported from various plants
and ecosystems (cf. Curtis and Wang 1998; Stitt
and Krapp 1999; Poorter and Pérez-Soba 2001;
Hoosbeek et al. 2002). In contrast with these
findings, Hoorens et al. (2003a) found significantly increased growth in response to CO2
enrichment in two graminoids from mesotrophic
peatland when grown at corresponding (‘mesotrophic’) nutrient availability. Therefore, our first
hypothesis is that the predominant vascular species in lowland Sphagnum –Phragmites reedlands,
which can penetrate into deeper, more nutrientrich soil layers, will show a significant increase in
productivity (as represented by abundance) in response to CO2 enrichment. Increasing dominance
of such plants could decrease the conservation
value of these rare ecosystems, if they were to
outcompete other vascular plants rooting in the
Sphagnum peat layer (e.g. orchid spp., Drosera
rotundifolia).
On the other side of the carbon balance, i.e. the
organic matter breakdown side, CO2-induced increases in productivity might result in greater
litter amounts entering the soil surface, which
may be an important contributor to changing soil
carbon dynamics (Norby and Cotrufo 1998). CO2
enrichment may have indirect effects on the
abiotics of peatlands (and thereby on the soil
decomposer communities), for instance CO2 induced plant species replacements or increased
water efficiency of extant species could change
the hydrology of the peatland (e.g. Heijmans
et al. 2001). In lowland Sphagnum –Phragmites
reedlands, of which the hydrology is tightly controlled by human management, we expect that
litter decomposition responses to CO2 enrichment, if any, would be related mostly to the
quantity and quality of the litter produced by
plants growing at ambient vs. elevated CO2 concentrations. Firstly, CO2 enrichment may change
litter quality via changes in species abundances,
given the knowledge that vascular peatland species may vary greatly in litter quality and
decomposability (Hoorens et al. 2003b; Quested
et al. 2003). Second, leaf litter decomposability of
a given species at elevated CO2 may differ from
that at ambient CO2 mostly because of: (1) dilution of nutrient concentrations of green leaves
due to increased storage of (mostly mobile, nonstructural) organic carbon (Poorter et al. 1997;
Curtis and Wang 1998; Saxe et al. 1998; Cornelissen et al. 1999); (2) a different pattern of
15
resorption of mineral nutrients (N, P) or carbon
compounds from senescing leaves. In a large
meta-analysis of CO2 responses in terms of
nutrient resorption efficiency and litter quality
and decomposability no consistent overall response patterns emerged, although a slight decline in litter N concentrations was seen in the
less realistic experimental set-ups (Norby et al.
2001a, see also van Heerwaarden 2004). However,
peatland species were hardly represented in these
datasets. Hoorens et al. (2003a) did find significantly reduced litter N concentrations and litter
respiration in the peatland sedge Carex rostrata
grown at elevated CO2 (but not in two other
vascular peatland species), while Robinson et al.
(1997) found either faster or slower decomposition of shoot litter from the subarctic peatland
grass Festuca vivipara grown at elevated CO2,
depending on the incubation environment. Here,
in addition to our first hypothesis outlined above,
we predict that the predominant vascular plants
in lowland Sphagnum reedland respond to CO2
enrichment by (a) higher C/N and C/P ratios of
green leaves; (b) similar N and P resorption
efficiencies resulting in higher leaf litter C/N and
C/P ratios and correspondingly lower leaf litter
decomposability.
We tested our hypotheses in a Dutch lowland
Sphagnum –Phragmites peatland using a relatively
non-intrusive in situ MINIFACE (Free air CO2
enrichment) system (Miglietta et al. 2001; Norby
et al. 2001b). In terms of uspscaling of our study
to CO2 responses of peatlands, these two-teer
ecosystems can provide insights into the general
responses of both oligotrophic (upland) and minerotrophic (lowland) peatlands.
Methods
Study area
We conducted our experiment in a lowland
Sphagnum –Phragmites reedland in the nature
reserve Het Guisveld, Westzaan, The Netherlands
(5229¢ N, 447¢ E. at sea level). These ecosystems
used to cover large areas in the northwestern
Netherlands, but only small pockets have remained to date. The climate in this region is
temperate-maritime, with annual precipitation at
780 mm distributed over all seasons. Mean temperature is 17 C in the warmest and 3 C in the
coldest month (1971 –2000, KNMI weather station at nearby Schiphol airport). The upper soil
profile of our experimental site hosts an approx.
50 cm thick Sphagnum peat layer, of which the
live part consists mostly of Sphagnum palustre L.,
S. recurvum var. mucronatum (Russ.) Warnst.
(=S. phallax Klingr.) and Polytrichum commune
Hedw. (the latter species expanding in recent
decades and during the course of our experiment). This layer is probably largely ombrotrophic. The predominant vascular plant is reed
Phragmites australis, which has its roots and
rhizomes mostly in the deeper layer below the
peat layer, which is muddy, more nutrient-rich
and fed at least partly by groundwater that is in
contact with canals and ditches draining the area.
Below the 50 –120 cm tall reed canopy other
predominant vascular species include the woody
species Rubus cf. fruticosus and Lonicera periclymenum; the grasses Calamagrostis canescens
and Anthoxanthum odoratum; the forb Hydrocotyle vulgaris; and the ferns Dryopteris carthusiana and D. cristata (for nomenclature of
vascular plants see van der Meijden 1996). Other
common vascular species include Cirsium palustre, Angelica sylvestris, Scirpus lacustris ssp. tabernaemontani, Dactylorrhiza praetermissa and
Thelypteris palustris, with occasional Drosera rotundifolia, Platanthera macrantha and Osmunda
regalis. The vegetation is mown once a year in
winter at 15 cm above the Sphagnum surface,
both in common regional reedland management
and in our experiment. This management also
partly halts strong potential encroachment by
shrubs and trees, although they do persist in the
system (e.g. Salix spp., Aronia prunifolia, Betula
pubescens, Sorbus aucuparia). The water table is
on average at 20 cm below the Sphagnum surface
(23 cm during autumn –winter, 18 cm during
spring –summer) but there is strong spatial variation within the site. There are visible gradients
of productivity (judging from plant heights and
densities) from the (more productive) northern
edge of the site near the main drainage canal to
the (lower productive) more central parts.
Slightly elevated, drier parts dominated by
Empetrum nigrum were excluded from the
experiment.
16
The MINIFACE experiment
Details of the experimental technology, design,
and management are in a companion paper
focusing on moss responses (Toet et al. In press)
and here we only give a summary description. Our
CO2 enrichment system (MINIFACE) was modified from Miglietta et al. (2001). Following a
randomised spatial design, there were six control
plots and six elevated CO2 plots, at minimum
distances of 7 m to avoid cross-contamination.
They were accessed via a board-walk system. It
was not possible to find 12 very similar plots initially, but both treatments appeared to have a
similar range of variation in productivity among
plots. In enrichment plots CO2 was injected into
ambient air that was vented out of two rows of 280
(1 mm diameter) holes each in a 1 m diameter ring
and, through a feedback system, maintained at
560 ppmv during daytime. Concentrations stayed
within 20% of this target for more than 95% of the
operational time and concentrations at 25 cm
from the inner edge of the rings deviated on
average less than 10% from those in the centre of
the plots. CO2 concentrations in the ambient plots,
which had the same rings, but venting ambient air
only, ranged generally between 360 and 400 ppmv
in daytime. Fumigation started on 26 April 2001
and continued throughout the study period until
January 2004, except for a break between 18
December 2001 and 22 March 2002 (before the
system was made frost-proof).
Plant abundance measurements
The abundance of each of the vascular plant species as well as litter in each plot was monitored
using the point-intercept method (modified from
Jonasson 1988), which tends to be an adequate
correlate of biomass (Jonasson 1988; Hobbie
1999). We lowered a 5 mm diameter steel pin rod
through each experimental plot at 121 points in a
grid with 5 cm distances (Figure 1). Thus, we
sampled within a 0.5 by 0.5 m square in the central
part of each plot. For each species at each point we
Figure 1. Point-intercept abundance measurements of vascular plant species in the Guisveld lowland Sphagnum –Phragmites reedland.
17
recorded the total number of hits of living leaves
or stems by the rod, and subsequently calculated
the total number of hits per plot. For litter we only
recorded the first hit, which we assumed to scale
with total amount at the plot level. The initial
recording was between 6 and 17 July 2000, i.e. in
the summer preceding the start of the CO2 fumigation treatment, and the second recording between 24 and 31 July 2003.
Leaf and litter chemistry and carbon isotope
signatures
Green leaf samples of three abundant species
(Phragmites, Rubus, Dryopteris carthusiana) were
collected from the plots in mid August 2002 and
litter samples of the same species between late
October and mid-December 2002. For some
ambient CO2 plots where target species were absent, complementary leaf and litter samples were
collected from plants within 1 m distance from the
plots. Leaf and litter samples were finely ground
and dried at 70 C for 48 h prior to chemical
analyses. For total C and N concentrations of the
three most abundant species, these samples were
subjected to dry combustion on a Perkin Elmer
2400 CHNS analyzer. Leaf P concentration was
measured colorimetrically (Murphy and Riley
1962) after digesting ground material in a 1:4
mixture of 37% (v/v) HCl and 65% HNO3 (as in
Sneller et al. 1999). C isotope compositions of
green leaf samples (of the same three species plus
Hydrocotyle and Lonicera) were determined using
an elemental analyser (Carlo Erba EA1110) coupled to an isotope ratio mass spectrometer (Thermo Finnigan Delta-Plus). Stable isotope
compositions are reported in the d notation:
d=(Rsample/Rstandard ) 1) 1000& where R represents 13C/12C. Isotopic results are reported relatively to VPDB. d13C of the enriched CO2 at the
source was determined on 27 May, 11 July, 28
November and 4 December 2003. We expected
isotope compositions in enriched plants to change
in the direction of the composition at the source.
Nutrient resorption efficiency
Nutrient resorption efficiency (RE) was defined as
100%* ([nutrient]green leaf – [nutrient]litter)/[nutri-
ent]green leaf In this formula the nutrient pool
([nutrient]) is commonly expressed on a leaf mass
basis, but this may produce significant deviations
from real resorption efficiency due to simultaneous
mass resorption during senescence (van Heerwaarden et al. 2003). We therefore also calculated
nutrient resorption efficiency with the nutrient
pool expressed on a leaf area basis (Delta-T area
meter, Cambridge, UK), for Phragmites and Rubus, which retained relatively stable leaf area. For
Dryopteris carthusiana, we expressed the nutrient
resorption efficiency on a (presumably stable) lignin basis because senescing leaf fronds tend to
shrivel up. See Rowland (1994) for lignin analysis.
Litter respiration assay
Four to six air-dried litter samples per species
(Phragmites, Rubus, Dryopteris carthusiana) and
treatment (each coming from a different MINIFACE ring) were used to assess litter decomposability. We followed the procedure described by
Aerts and De Caluwe (1997) and Hoorens et al.
(2002), which estimates litter decomposability by
measuring microbial respiration rates during initial decomposition under standardized, optimal
laboratory conditions. The samples were remoistened for 24 h in a filtrate of a mixture of soil and
litter from the study site to promote the local
microbial community, and to fully hydrate the
litter. Each remoistened sample was placed in a
100 ml glass jar. In order to keep jar air humidity
as high as possible, 10 ml of a potassium sulphate
buffer solution was added to each jar. Some glass
marbles were subsequently placed in the buffer so
that the top marbles emerged from the solution. A
mesh (to host the litter samples) was placed on the
top of the marbles, to avoid direct contact between
the buffer solution and the samples. The top of the
jars was left open to permit free air circulation
between the jar and the incubation environment.
The jars were randomly arranged in laboratory
trays, and placed in a climate room at 20 C in the
dark, and relative humidity at 95%. Five additional jars without litter were also included in the
trays. When necessary (any signs of the samples
drying out), we remoistened the samples adding
distilled water with a syringe directly to the litter.
The litter was incubated for 66 days. During this
period, we measured net CO2 production rate
18
every 7 –12 days as follows. The jars were sealed
with a lid carrying a silicon septum, and one gas
sample of 25 ll was taken from the jar atmosphere
with a syringe penetrating the septum. In the gas
sample, CO2 concentration was measured with a
Hewlett Packard 5890 gas chromatograph equipped with a thermal conductivity detector. After 4 h
of CO2 build-up in the air-tight jars, CO2 concentration was measured again. The change in
CO2 concentration during that time period was
assumed to be due to microbial respiration. CO2
concentration was corrected for the CO2 dissolved
in the buffer solution (Stumm and Morgan 1981),
for the air volume extracted with the syringe
(50 ll), and for the residual CO2 production
measured in the five jars without litter. Litter respiration rates were expressed as mg CO2 g l)1 h)1.
Total estimated CO2 production per gram of litter
in each jar throughout the 66 days period of the
experiment (mg CO2 g l)1) was calculated by
Newton integration, after the average CO2 production respiration rate for each time interval between two measuring dates had been computed.
Statistical analyses
Point-intercept abundance data by species were
log(x + 1) transformed before analyses in order
to account for zero values and to improve homogeneity of variances. We subjected these to a threeway repeated measures analysis of variance
(ANOVA) with species (the five with occurrence in
a sufficient number of plots: Phragmites, Calamagrostis, Anthoxanthum, Rubus, Hydrocotyle)
and CO2 treatment as between-subject factors and
year (2000 vs. 2003) as the within-subject factor. A
combination of a CO2 effect and a CO2 *year
interaction would be interpreted as a significant
overall CO2 response, while the combination of a
CO2 effect and a species *CO2 *year interaction
would be interpreted as a possible CO2 response of
one or more species. With a similar rationale, logtransformed data for the total number of live
vascular plant hits or litter hits per plot were
subjected to a two-way repeated measures ANOVA, with CO2 as between-subjects and year as
within-subjects factor.
To test for treatment effects on d13C signatures,
on the chemistry of green leaves and litter, on
nutrient resorption efficiency, and on litter
respiration rates, two-way ANOVAs with treatment and species as fixed factors were performed
for each variable. We explored the relationship
between litter chemistry and litter decomposability
by simple linear regressions between C:N or C:P
ratios and total CO2 production. Prior to the
analyses, normality and homoscedasticity were
checked. d13C signatures had to be log()x)
transformed and percentage data were arcsine
[square-root(X/100)] transformed where necessary
to improve variance homogeneity. All statistical
analyses were carried out using SPSS 11.0.
Results
Plant abundance varied significantly among
species (Table 1, F=21.7, p<0.001). However, the
three-way repeated measures ANOVA revealed no
significant effect of CO2 (F=0.036, p=0.85), CO2
*year (F=0.562, p=0.69) or species *CO2 *year
interaction (F=0.405, p=0.80). The two-way repeated measures ANOVAs for total vascular plant
abundance (CO2: F=0.462, p=0.51, CO2 *year:
F=0.482, p=0.48) or for litter abundance (CO2:
F=0.027, p=0.87, CO2 *year: F=1.55, p=0.24)
did not reveal any significant CO2 effects on
abundance either. The apparently greater total
vascular plant abundance after CO2 treatment
(Table 1) could partly be attributed to the expansion of patches of Rubus, Lonicera or Dryopteris
carthusiana in some of the plots (authors’ unpublished data) and was not necessarily related to CO2
enrichment. Thus, no obvious CO2 enrichment
effects on vascular plant or litter abundance were
detected at all. Correspondingly, there were no
CO2 enrichment effects on vascular plant species
richness (initial in July 2000: ambient treatment
8.3 ± 0.3, CO2 enrichment 9.0 ± 0.5 species per
plot; July 2003: ambient 8.3 ± 0.6, CO2 8.5 ± 0.5
species per plot).
Foliar d13C values were consistently lower
in CO2 enriched plots than in ambient plots
(Figure 2). While all individual species showed this
pattern, the significant Species *CO2 interaction
supports the observation that one species, i.e.
Phragmites australis, had a smaller difference in
d13C values between treatments than others. This
may be attributed to the elevated position of
Phragmites leaves, which probably experienced
lower CO2 concentrations than the 560 ppmv
19
Table 1. Point intercept abundance (number of hits) of the main vascular plant species and total vascular plant litter in Summer 2003
and the change in abundance (difference in number of hits) between both recordings. SE, standard error of the mean; N, number of
plots. Plots in which the species was absent were included in Summer 2000 (data not shown) and Summer 2003 (zero values), but plots
in which a species was absent at both recordings were not used to calculate change in abundance. In each plot a 0.25 m2 square was
sampled.
Summer 2003
Ambient
Elevated CO2
Mean
SE
N
Mean
SE
N
Phragmites australis
Anthoxanthum odoratum
Calamagrostis canescens
Hydrocotyle vulgaris
Rubus cf. fruticosus
Total hits vascular plants
Litter from vascular plants
123
4
3
40
8
199
46
38
1
2
27
5
48
6
6
6
6
6
6
6
6
103
3
1
18
43
297
66
28
2
1
15
28
97
13
6
6
6
6
6
6
6
Summer 2003 – Summer 2000 Change
Phragmites australis
Anthoxanthum odoratum
Calamagrostis canescens
Hydrocotyle vulgaris
Rubus cf. fruticosus
Total hits vascular plants
Litter from vascular plants
49
)8
)16
13
4
64
7
36
4
30
35
5
61
8
6
6
2
4
4
6
6
49
)9
3
1
37
139
31
28
8
2
15
31
79
15
6
5
2
5
4
6
6
Figure 2. Response of d13C of green leaves of five vascular
plant species to CO2 enrichment. Standard errors of the means
are shown one-sided only. Results of two-way ANOVA:
Species: F=35.5, p<0.001; CO2: F=539.7, p<0.001; Species *
CO2: F=3.28, p=0.023.
maintained lower down. For the other four species, the differences between treatments deviated
only little from the calculated expected difference
of 7.7& based on the contribution of enriched
CO2 to the total CO2 supply in enriched plots
((560 –380)/560), where ambient CO2 had an
approximate d13C value of )8& and enriched CO2
of )31.9 ± 2.1& (see also Toet et al. In press).
In green leaves of the three focal species
(Phragmites, Rubus, Dryopteris carthusiana) [N]
and [P] were generally lower and C/N ratios and
C/P ratios generally higher in CO2 enrichment
plots than in ambient plots (Table 2), although the
significant CO2 * Species interaction for C/P could
be attributed to Phragmites not showing a CO2
response (data not shown). Two further species
with poorer replication (Hydrocotyle, Lonicera)
showed similarly reduced [N] and [P] and higher
C/N and C/P ratios in green leaves of CO2 enriched plants (data not shown). Such a chemical
CO2 response was no longer detectable in leaf litter
of the same species from the same plots, except for
litter C/N ratio which was still somewhat higher in
elevated CO2 plots (Table 2), mainly owing to the
contribution of Dryopteris carthusiana. The difference in response for green leaves and litter
translated into lower mass-based resorption efficiency in response to CO2 enrichment, both for N
and P, but there was no significant CO2 effect
(only a trend) on area-based N or P resorption
efficiency (Table 2, Figure 3). Area-based resorption efficiencies were on average 15% higher than
mass-based ones in both treatments.
20
Table 2. Results of two-way ANOVAs on variables relation to leaf and litter chemistry, nutrient resorption efficiency and respiration,
with fixed factors CO2 treatment and species (Phragmites australis, Rubus cf. fruticosus, Dryopteris carthusiana). * p<0.05; **p<0.01;
***p<0.001; ns, not significant. Codes are as follows:
Ng
Pg
Nl
Pl
C/Ng
C/Pg
C/Nl
C/P(a)
l
N rm
P rm
N r(b)
A
(b)
P r(a)
A
Lrespiration
CO2 Effect Sign
CO2
Species
CO2*Sp.
Error df
–
–
***
**
ns
ns
***
*
*
ns
*
**
ns
ns
ns
***
**
ns
*
***
**
ns
**
**
***
***
**
ns
ns
*
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
17
16
18
18
17
16
18
18
16
16
15
15
18
+
+
+
)
)
Ng, N% in green leaves; Nl,N% in litter; Pg, P% in green leaves; Pl, P% in litter; C/Ng, C/N ratio in green leaves; C/Pg, C/P ratio in
green leaves; C/Nl, C/N ratio in litter; C/Pl, C/P ratio in litter; Nrm, N resorption efficiency (mass basis); Prm, P resorption efficiency
(mass basis); Nra, N resorption efficiency (area basis); Pra, P resorption efficiency (area basis); Lrespiration, Cumulative CO2 production
over 66 days (mg CO2/g litter).
Figure 3. Mass and area based nutrient resorption efficiency.
Dark bars: N resorption efficiency, white bars: P resorption
efficiency. Horizontal axis: Dc, Dryopteris carthusiana; Pa,
Phragmites australis; Rf, Rubus cf. fruticosus; a – ambient CO2;
e – elevated CO2 concentration. For the bottom graph,
resorption in Dc was calculated on a lignin basis, in Pa and RF
on an area basis. Standard errors are shown one-sided. See
Table 2 for statistical analyses.
There was no significant CO2 effect on litter
respiration for any of the three species investigated
(Table 2), neither for patterns over time (data not
shown) nor for cumulative CO2 production
(Figure 4). There was no relationship between
initial litter C/N ratio and cumulative CO2 production (negative slope, R2=0.11, p=0.11) or
between initial litter C/P ratio and cumulative CO2
Figure 4. Cumulative CO2 production due to initial respiration
(66 days) of litter collected from ambient and elevated CO2
plots during incubation under laboratory conditions. Horizontal axis: Dc, Dryopteris carthusiana; Pa, Phragmites australis; Rf, Rubus cf. fruticosus; a – ambient CO2; e – elevated
CO2 concentration. Standard errors are shown one-sided. See
Table 2 for statistical analyses.
production (R2< 0.01, p=0.88), irrespective of the
CO2 treatment.
Discussion
The most striking finding from this 3-year experimental study in a Dutch lowland Sphagnum –
Phragmites peatland was the lack of CO2 response
of the vascular vegetation component, both on the
production (gains) and on the ‘destruction’ (losses)
21
side of the organic carbon balance. This is particularly striking in view of the clear empirical evidence that the vegetation had taken up and
processed the extra 180 ppmv of CO2 supplied by
our MINIFACE enrichment. This evidence was
provided by the consistently lower d13C signatures
and higher C/N and C/P ratios of green leaves of
some of the predominant vascular plant species in
CO2 enriched plots. Below we shall discuss some of
the factors that may together explain the lack of
vegetation response to CO2 in this study.
Contrary to our first hypothesis, we did not
detect plant abundance responses and presumably,
therefore, biomass responses (see Methods).
Hoosbeek et al. (2002) found the same pattern
analyzing vascular plants from several ombrotrophic bogs in NW Europe, and argued that low
availability of K or P could limit the potentially
fertilizing effect of elevated CO2. However, in our
minerotrophic system, nutrient availability should
not have posed such a limiting effect, and the lack
of response may be attributed to several other
factors acting together. Firstly, the higher C/N and
C/P ratios of green leaves in CO2 enriched plots,
combined with the apparently mobile nature of the
additional carbon as deduced from increased mass
resorption (sensu van Heerwaarden et al. 2003)
during senescence at high CO2 (affirmative data
not shown), together point towards predominant
storage of the surplus carbon as non-structural
carbohydrates (starch). This has also been found
in many previous studies (for reviews see Poorter
et al. 1997; Curtis and Wang 1998, Körner 2000).
Carbon that is translocated from the leaves to
other plant parts may be processed for growth in
subsequent years, for instance in periods of
assimilate limitation due to shading, but it will
contribute little or not at all to further plant
growth in the shorter term. Second, annual winter
mowing at 15 cm above the Sphagnum carpet removed not only litter, but also some living perennial shoots of woody and semi-woody plants such
as Rubus and Lonicera. This could have reduced
the overall biomass accumulation of such species.
At the same time, this mowing regime does represent the typical management for this ecosystem,
also in other areas. Third, we can not rule out
experimental artifacts that could have obscured
CO2 effects on vegetation productivity. Our site
was spatially most heterogeneous, with clear
internal gradients in water tables (Toet et al. In
press), productivity (visual observations) and species composition. Combined with logistic constraints such as (a) minimum distances between
plots to prevent CO2 contamination of control
plots and (b) small plot size relative to the large
size, clonal habit and patchiness of the predominant plants, this resulted inevitably in substantial
initial variability among plots. We can not exclude
the possibility that this heterogeneity has obscured
an underlying trend of greater productivity under
CO2 enrichment. At the same time, the spatial
heterogeneity is a real characteristic of this ecosystem type. Besides employing more and larger
plots, longer time periods for CO2 response of the
vegetation would be recommendable too, in view
of the apparent substantial belowground resource
storage of the clonal plants (pre-treatment ‘memory’) and possible feedbacks provided by longterm CO2-induced soil responses.
On the ‘destruction’ side of the ecosystem carbon balance, viz. the decomposition pathway, the
lack of clear CO2 responses was similarly obvious.
Firstly, litter quantity (i.e. litter abundance as
point-intercept hits), which largely determines how
much organic matter could potentially be decomposed, did not differ significantly between ambient
and elevated CO2 treatments. Second, litter quality, which determines the rate at which this organic
matter can be decomposed, showed little significant CO2 response other than a somewhat higher
C/N ratio in Dryopteris carthusiana (and Hydrocotyle vulgare; data not shown) in enriched plots,
similar to the findings of Hoosbeek et al. (2002) in
ombrotrophic bogs. Although the N and P concentrations of green leaves were lower and C/N
and C/P ratios higher in CO2 plots, in support of
our second hypothesis, this chemical response was
partly cancelled out by resorption of presumably
mobile carbohydrates during leaf senescence. As a
consequence, leaf litter quality was somewhat
convergent between both treatments, which is at
odds with our third hypothesis. Our findings seem
to correspond with the current body of literature,
where green leaf N concentrations are generally
lower and C/N ratios higher in response to CO2
enrichment (Poorter et al. 1997; Cotrufo et al.
1998; Curtis and Wang 1998; Cornelissen et al.
1999; Hoorens et al. 2003a), while the same
responses (lower [N], higher C/N) are much less
consistent and less strong in leaf litter (Norby
et al. 2001a). It seems therefore that differences in
22
resorption pattern are an important moderating
factor in the translation from green plant responses to CO2 enrichment to responses of leaf
litter and their decomposition. If ‘surplus’ mobile
carbon is diverted towards perennial structures
(e.g rhizhomes, wood) of long-lived plants, adding
to their year-to-year biomass, their changing potential for C sequestration would be partly a
function of carbon and nutrient resorption from
senescing leaves.
Indeed, a large meta-analysis of CO2 enrichment studies covering various biomes (Norby
et al. 2001a) revealed that there was an overall
average reduction of litter N concentration of
7.1%, but this was not seen in the subset of
experiments where litter was collected from in situ
CO2 exposure such as ours. Hoorens et al. (2003a)
found significantly lower litter N concentrations
and higher C/N ratios in CO2-enriched plants in
three out of five vascular plant species (and one
species with a trend in the same direction of response), but the plants from which their leaf litter
was derived had been grown and enriched in
greenhouses.
The total lack of CO2 response of litter respiration was at odds with our third hypothesis (see
Introduction). However, this can not automatically be interpreted as the consequence of the small
and inconsistent response of litter quality, because
litter C/N or C/P ratios were no correlates of litter
respiration across all three species and treatments.
This is surprising, provided that, in our type of
litter respiration set-up, no other factors than litter
chemistry are supposed to influence decomposition. It is likely that the allocation of C to secondary compounds vs. carbohydrates, and
consequently parameters such as Lignin content or
Lignin/N, are the litter chemistry factors that are
really controlling litter decomposition rates (Aerts
1997). Similarly, Norby et al. (2001a) in their
meta-analysis found no CO2 effect on litter
decomposability whether measured as mass loss or
as respiration, in spite of the on average lower N
concentrations in CO2-enriched litters. In contrast,
Hoorens et al. (2003a) in a smaller meta-analysis
did find that a CO2 induced reduction of litter N
correlated with a reduction in litter decomposition
(measured as mass loss or respiration). However,
in the latter, a substantial proportion of the studies
involved had derived litter from plants grown and
enriched in less natural settings.
Conclusions
When combining our findings with those from
other in situ MINIFACE experiments with CO2
enrichment in temperate or boreal Sphagnumdominated peatlands (Berendse et al. 2001;
Hoosbeek et al. 2001; Heijmans et al. 2002), our
preliminary conclusion is that vascular vegetation
in these ecosystems is not very responsive to CO2.
Indirect longer term responses via changes in the
Sphagnum turf, e.g. Polytrichum moss outcompeting Sphagnum (Toet et al. In press) should
however not be ruled out as yet. At least in the
shorter to medium term, any possible CO2 effects
will probably be very small compared to other
anthropogenic environmental changes. The composition and functioning of Sphagnum peatlands
are very strongly dependent on local and regional
hydrology and water quality (e.g. Glaser et al.
1990; Moore et al. 2002), both of which are under
strong control of human management, at least in
many temperate regions and especially in The
Netherlands. Also, high N deposition is known to
drastically alter such peatlands, as evidenced for
instance by vascular plant increases in a fertilized
Dutch peat bog (Heijmans et al. 2002). Moreover,
in the real (future) world the ‘greenhouse effect’
comprises both higher atmospheric CO2 concentrations and higher temperatures simultaneously
and the interaction of the two factors (in combination with variation in hydrology and N deposition) may perhaps produce different vegetation
responses if studied experimentally in situ (see
Norby and Luo 2004).
The composition, productivity and functioning
of most of the lowland Sphagnum –Phragmites
reedlands, like the one under study here, also
depend strongly on the timing, frequency and
intensity of reed mowing, on whether this is
done manually or by heavy vehicles compacting
the Sphagnum foundation, and on whether and
how frequently trees and shrubs are pulled out
of the soil. All these measures are aimed at
arresting the relatively early successional phase
of these peatlands in order to preserve biodiversity. It is likely that a cessation of such
management, resulting in a development towards
woodland within several decades, would alter
carbon sequestration and processing more than
the extra atmospheric carbon availability on a
similar time scale.
23
Acknowledgements
We thank the Dutch Forestry Authority (Staatsbosbeheer, Alkmaar office) for allowing us to use
their land and facilities, and particularly the
Guisveld wardens, Erik Gerrevink and Wouter
Maatje, for all their help, hospitality and anecdotes. Rob Stoevelaar, Cor Stoof, Martin vanVilsteren and co-workers helped with the
development and maintenance of the FACErelated equipment. Ellen Dorrepaal and Bart
Hoorens helped with the litter respiration work
and Miranda de Beus, Adrie van Beem, Martin
Stroetenga and Nancy de Bakker with some of the
fieldwork. Thanks to all.
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